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Smith, B. T.

Publications and source records attributed to Smith, B. T..

15 recordsLinked to original sources

Ancient mitogenomes reveal unexpected diversity in Madagascar's extinct hippopotamuses

Madagascar's extinct hippopotamuses were a distinctive component of the island's recently lost megafauna, yet their origins, diversification history, and taxonomy have remained unresolved. Here, we recover the first ancient mitochondrial genomes from Malagasy hippopotamuses, obtaining phylogenetic data from 37 subfossil specimens across seven localities and all three named species, and integrate these data with morphology and total-evidence phylogenetic analyses. The 35 endemic specimens form a single clade most closely related to Hippopotamus amphibius, supporting a single colonization of Madagascar. Within this radiation, five deeply divergent and geographically structured mitochondrial lineages diversified across most regions of Madagascar during the Pleistocene. Tip-dating estimates a remarkably young crown age of ~1.41 Ma, following divergence from mainland Hippopotamus at ~3.24 Ma. These lineages do not map cleanly onto traditional taxonomy: material assigned to H. lemerleispans several divergent clades, while H. laloumena and H. madagascariensis are nested within this broader diversity. Morphology supports some lineage assignments but also points to previously unrecognized diversity, while ancestral-state reconstruction supports early body-size reduction followed by a secondary increase in H. laloumena. Malagasy hippopotamuses therefore represent an exceptionally recent radiation of large-bodied island mammals (and the youngest in Madagascar), showing that Madagascar continued to generate endemic mammalian diversity well into the Pleistocene. Their late-Holocene extinction erased the product of more than a million years of rapid insular diversification, the drivers of which remain enigmatic.

evolutionary biology↗

Metabolic reprogramming by caloric restriction enhances acute phase virological control and reduces chronic inflammation in SIV-infected rhesus macaques

Nutrient metabolism influences HIV-1 replication, antiviral immunity, and chronic inflammation, yet is difficult to leverage for therapeutic gain. We sought to modulate metabolism in the non-human primate model of HIV-1 by caloric restriction (CR), a modality canonically known for its antiaging benefits. Four months of 30% CR was safe and resulted in broad and systemic metabolic reprogramming in healthy adult male and female rhesus macaques. Relative to that of ad libitum-fed animals, CR lowered the frequencies of target CCR5+ CD4 T cells in the gut mucosa. Upon infection with SIV, CR reduced acute phase viremia, dampened type I interferon signaling, and overall permitted a more vigorous cycling of CD8+ T cells in lymphoid tissues. CR-induced protection from SIV was associated with a robust up-regulation of glycolysis, which supported an early reduction in viremia that ultimately waned over time. During virologic suppression with antiretroviral therapy (ART), CR significantly limited gastrointestinal (GI) immune activation, improved tricarboxylic acid cycle flux, and lowered concentrations of soluble CD14 and several TNF-related molecules in plasma. Blood SIV DNA levels however were unchanged by CR, suggesting that residual GI dysfunction and inflammation can be decoupled from viral persistence. Our findings highlight that a dietary modality can limit pathology in a primate lentiviral infection. They also reveal the robust but temporally constrained nature of glycolysis in supporting an acute antiviral response. SIGNIFICANCECaloric restriction (CR) is a safe dietary intervention known to confer anti-aging and health benefits across diverse animal models. However, its application in the context of infectious diseases has yielded mixed outcomes and has largely been limited to murine systems. In this study, we therefore employed CR to examine the impact of dietary modulation on SIV infection outcomes. Our findings demonstrate that CR reduced acute-phase viremia and attenuated markers of chronic inflammation following ART, effects that were associated with distinct metabolic signatures. Collectively, these findings underscore the importance of diet and nutrition in shaping chronic viral infection outcomes, such as SIV, within a clinically relevant non-human primate model.

immunology↗

Efficient Inference of Macrophylogenies: Insights from the Avian Tree of Life

The exponential growth of molecular sequence data over the past decade has enabled the construction of numerous clade-specific phylogenies encompassing hundreds or thousands of taxa. These independent studies often include overlapping data, presenting a unique opportunity to build macrophylogenies (phylogenies sampling > 1,000 taxa) for entire classes across the Tree of Life. However, the inference of large trees remains constrained by logistical, computational, and methodological challenges. The Avian Tree of Life provides an ideal model for evaluating strategies to robustly infer macrophylogenies from intersecting datasets derived from smaller studies. In this study, we leveraged a comprehensive resource of sequence capture datasets to evaluate the phylogenetic accuracy and computational costs of four methodological approaches: (1) supermatrix approaches using concatenation, including the "fast" maximum likelihood (ML) methods, (2) filtering datasets to reduce heterogeneity, (3) supertree estimation based on published phylogenomic trees, and (4) a "divide-and-conquer" strategy, wherein smaller ML trees were estimated and subsequently combined using a supertree approach. Additionally, we examined the impact of these methods on divergence time estimation using a dataset that includes newly vetted fossil calibrations for the Avian Tree of Life. Our findings highlight that recently developed fast tree search approaches offer a reasonable compromise between computational efficiency and phylogenetic accuracy, facilitating inference of macrophylogenies.

evolutionary biology↗

Genomes of the extinct Bachman's Warbler shows high divergence and no evidence of admixture with other extant Vermivora Warblers

Bachmans Warbler (Vermivora bachmanii) - last sighted in 1988 - is one of the few North American passerines that have gone extinct. Given the extensive ongoing hybridization of its two extant congeners - the Blue-Winged Warbler (V. cyanoptera) and Golden-Winged Warbler (V. chrysoptera) - and shared patterns of plumage variation between Bachmans Warbler and hybrids between those extant species, it has been suggested that Bachmans Warbler might have also had a component of hybrid ancestry. Here, we use historic DNA (hDNA) and whole genome sequencing of Bachmans Warblers collected at the turn of the 20th century to address this possibility. We combine these data with genomes of the two extant Vermivora species to examine patterns of population differentiation, inbreeding, and gene flow. In contrast to the admixture hypothesis, the genomic evidence is consistent with V. bachmanii being a highly divergent, reproductively isolated species, with no evidence of introgression. We show that both V. bachmanii and V. chrysoptera have elevated runs of homozygosity compared to V. cyanoptera, consistent with the effects of a small effective population size or population bottlenecks in the former two species. We also found--using population branch statistic estimates of all three species--previously undocumented evidence of lineage-specific evolution in V. chrysoptera near a novel pigmentation gene candidate for warblers, CORIN, which is a known modifier of ASIP, which is in turn involved in melanic throat and mask coloration in this family of birds. Together, these genomic results also highlight how natural history collections are such invaluable repositories of information about extant and extinct species. SignificanceFew common North American passerines have gone extinct. Bachmans Warbler is, unfortunately, one that has--the last sighting was in 1988. Here we use whole genome historical DNA from museum specimens of Bachmans warblers collected at the turn of the 20th century to learn about the evolution of this species and test whether there was evidence for hybridization and gene flow between it and two extant members of the same genus which, today, hybridize extensively. We find Bachmans warbler was highly divergent with no evidence of gene flow. We also find evidence of elevated "runs of homozygosity" in both Bachmans warbler and one of the two extant Vermivora species, suggesting the effects of a small population size or population bottlenecks.

evolutionary biology↗

Population genomics of the island thrush elucidates one of earth's great archipelagic radiations

Tropical islands are renowned as natural laboratories for evolutionary study. Lineage radiations across tropical archipelagos are ideal systems for investigating how colonization, speciation, and extinction processes shape biodiversity patterns. The expansion of the island thrush across the Indo-Pacific represents one of the largest yet most perplexing island radiations of any songbird species. The island thrush exhibits a complex mosaic of pronounced plumage variation across its range, and is arguably the worlds most polytypic bird. It is a sedentary species largely restricted to mountain forests, yet it has colonized a vast island region spanning a quarter of the globe. We conducted comprehensive sampling of island thrush populations and obtained genome-wide SNP data, which we used to reconstruct its phylogeny, population structure, gene flow, and demographic history. The island thrush evolved from migratory Palearctic ancestors and radiated explosively across the Indo-Pacific during the Pleistocene, with numerous instances of gene flow between populations. Its bewildering plumage variation masks a biogeographically intuitive stepping stone colonization path from the Philippines through the Greater Sundas, Wallacea and New Guinea to Polynesia. The island thrushs success in colonizing Indo-Pacific mountains can be understood in light of its ancestral mobility and adaptation to cool climates; however, shifts in elevational range, degree of plumage variation and apparent dispersal rates in the eastern part of its range raise further intriguing questions about its biology.

evolutionary biology↗

The genomic landscapes of desert birds are structured by contemporary features

Spatial models show that genetic differentiation between populations can be explained by factors ranging from geographic distance to environmental resistance across the landscape. However, genomes exhibit a landscape of differentiation, which could indicate that multiple spatial models better explain divergence in different portions of the genome. We test whether alternative geographic predictors of intraspecific differentiation vary across the genome in ten bird species that co-occur in Sonoran and Chihuahuan Deserts of North America. Using population-level genomic data, we characterized the genomic landscapes across species and modeled five predictors that represented historical and contemporary mechanisms. The characteristics of genomic landscapes differed across the ten species, influenced by varying levels of population structuring and admixture between deserts. General dissimilarity matrix modeling indicated that the best-fit models differed from the whole genome and partitions along the genome. Almost all of the historical and contemporary mechanisms were important in explaining genetic distance, but particularly historical and contemporary environment, while contemporary abundance, position of the barrier to gene flow, and distance explained relatively less. Individual species have significantly different patterns of genomic variation. These results illustrate that the genomic landscape of differentiation was influenced by alternative geographic factors operating on different portions of the genome.

evolutionary biology↗

Demography and linked selection interact to shape the genomic landscape of codistributed woodpeckers during the Ice Age

The glacial cycles of the Pleistocene had a global impact on the evolution of species. Although the influence of genetic drift on population genetic dynamics is well understood, the role of selection in shaping patterns of genomic variation during these dramatic climatic changes is less clear. We used whole genome resequencing data to investigate the interplay between demography and natural selection and their influence on the genomic landscape of Downy and Hairy Woodpecker, species co-distributed in previously glaciated North America. Our results revealed a dynamic population history with repeated cycles of bottleneck and expansion, and genetic structure associated with glacial refugia. Levels of nucleotide diversity varied substantially along the genomes of Downy and Hairy Woodpecker, but this variation was highly correlated between the two species, suggesting the presence of conserved genomic features. Nucleotide diversity in both species was positively correlated with recombination rate and negatively correlated with gene density, suggesting that linked selection played a role in reducing diversity in regions of low recombination and high density of targets of selection. Despite strong temporal fluctuations in Ne, our demographic analyses indicate that Downy and Hairy Woodpecker were able to maintain relatively large effective population sizes during glaciations, which might have favored natural selection. The magnitude of the effect of linked selection seems to have been modulated by the individual demographic trajectory of populations and species, such that purifying selection has been more efficient in removing deleterious alleles in Hairy Woodpecker owing to its larger long-term Ne. These results highlight that while drift captures the expected signature of contracting and expanding populations during climatic perturbations, the interaction of multiple processes produces a predictable and highly heterogeneous genomic landscape.

evolutionary biology↗

Genomic architecture controls spatial structuring in Amazonian birds

Large rivers are ubiquitously invoked to explain the distributional limits and speciation of the Amazon Basins mega-diversity. However, inferences on the spatial and temporal origins of Amazonian species have narrowly focused on evolutionary neutral models, ignoring the potential role of natural selection and intrinsic genomic processes known to produce heterogeneity in differentiation across the genome. To test how genomic architecture impacts our ability to reconstruct patterns of spatial diversification across multiple taxa, we sequenced whole genomes for populations of bird species that co-occur in southeastern Amazonian. We found that phylogenetic relationships within species and demographic parameters varied across the genome in predictable ways. Genetic diversity was positively associated with recombination rate and negatively associated with the species tree topology weight. Gene flow was less pervasive in regions of low recombination, making these windows more likely to retain patterns of population structuring that matched the species tree. We further found that approximately a third of the genome showed evidence of selective sweeps and linked selection skewing genome-wide estimates of effective population sizes and gene flow between populations towards lower values. In sum, we showed that the effects of intrinsic genomic characteristics and selection can be disentangled from the neutral processes to elucidate how speciation hypotheses and biogeographic patterns are sensitive to genomic architecture.

genomics↗

River network rearrangements promote speciation in lowland Amazonian birds

Large Amazonian rivers impede dispersal for many species, but lowland river networks frequently rearrange, thereby altering the location and effectiveness of river-barriers through time. These rearrangements may promote biotic diversification by facilitating episodic allopatry and secondary contact among populations. We sequenced genome-wide markers to evaluate histories of divergence and introgression in six Amazonian avian species-complexes. We first tested the assumption that rivers are barriers for these taxa and found that even relatively small rivers facilitate divergence. We then tested whether species diverged with gene flow and recovered reticulate histories for all species, including one potential case of hybrid speciation. Our results support the hypothesis that river dynamics promote speciation and reveal that many rainforest taxa are micro-endemic, unrecognized and thus threatened with imminent extinction. We propose that Amazonian hyper-diversity originates in part from fine-scale barrier displacement processes -including river dynamics- which allow small populations to differentiate and disperse into secondary contact.

evolutionary biology↗

Comparative phylogeography reveals how a barrier filters and structures taxa in North American warm deserts

The study of biogeographic barriers have been instrumental in understanding the evolution and distribution of taxa. Now with the increased availability of empirical datasets, it is possible to infer emergent patterns from communities by synthesizing how barriers filter and structure populations across species. We assemble phylogeographic data for a barrier and perform spatially-explicit simulations to quantify temporal and spatial patterns of divergence, the influence of species traits on these patterns, and understand the statistical power of differentiating alternative diversification modes. We incorporate published datasets to examine taxa around the Cochise Filter Barrier, separating the Sonoran and Chihuahuan deserts of North America, to synthesize phylogeographic structuring across the community with respect to organismal functional traits. We then use a simulation and machine learning pipeline to assess the power of phylogeographic model selection. Taxa distributed across the Cochise Filter Barrier show heterogeneous responses to the barrier in levels of gene flow, phylogeographic structure, divergence timing, barrier width, and divergence mechanism. These responses vary concordantly with locomotor and thermoregulatory traits. Many taxa show a Pleistocene population genetic break, often with introgression after divergence. Allopatric isolation and isolation-by-environment are the primary mechanisms purported to structure taxa. Simulations reveal that in spatially-explicit isolation-with-migration models across the barrier, age of divergence, presence of gene flow, and presence of isolation-by-distance can confound the interpretation of evolutionary history and model selection by producing easily-confusable results. By synthesizing phylogeographic data for the Cochise Filter Barrier we show a pattern where barriers interact with species traits to differentiate taxa in communities over millions of years. Identifying the modes of differentiation across the barriers for these taxa remains challenging because commonly invoked demographic models may not be identifiable across a range of likely parameter space.

evolutionary biology↗

Bursts and constraints generate a rainbow in the lorikeets

BackgroundBird plumage exhibits a diversity of colors that serve functional roles ranging from signaling to camouflage and thermoregulation. However, birds must maintain a balance between evolving colorful signals to attract mates, minimizing conspicuousness to predators, and optimizing adaptation to climate conditions. Examining plumage color macroevolution provides a framework for understanding this dynamic interplay over phylogenetic scales. Plumage evolution due to a single overarching process, such as selection, may generate the same macroevolutionary pattern of color variation across all body regions. In contrast, independent processes may partition plumage into sections and produce region-specific patterns. To test these alternative scenarios, we collected color data from museum specimens of an ornate clade of birds, the Australasian lorikeets, using visible-light and UV-light photography, and comparative methods. We predicted that the diversification of homologous feather regions, i.e., patches, known to be involved in sexual signaling (e.g., face) would be less constrained than patches on the back and wings, where new color states may come at the cost of crypsis. Because environmental adaptation may drive evolution towards or away from color states, we tested whether climate more strongly covaried with plumage regions under greater or weaker macroevolutionary constraint.\n\nResultsWe found that alternative macroevolutionary models and varying rates best describe color evolution, a pattern consistent with our prediction that different plumage regions evolved in response to independent processes. Modeling plumage regions independently, in functional groups, and all together showed that patches with similar macroevolutionary models clustered together into distinct regions (e.g., head, wing, belly), which suggests that plumage does not evolve as a single trait in this group. Wing patches, which were conserved on a macroevolutionary scale, covaried with climate more strongly than plumage regions (e.g., head), which diversified in a burst.\n\nConclusionsOverall, our results support the hypothesis that the extraordinary color diversity in the lorikeets was generated by a mosaic of evolutionary processes acting on plumage region subsets. Partitioning of plumage regions in different parts of the body provides a mechanism that allows birds to evolve bright colors for signaling and remain hidden from predators or adapt to local climatic conditions.

evolutionary biology↗

Uneven missing data skews phylogenomic relationships within the lories and lorikeets

The resolution of the Tree of Life has accelerated with advances in DNA sequencing technology. To achieve dense sampling, it is often necessary to obtain DNA from historical museum specimens to supplement modern genetic samples. However, DNA from historical material is generally degraded and fragmented, which presents various challenges. In this study, we evaluated how the coverage at variant sites and missing data among historical and modern sample types impacts phylogenomic inference. We explored these patterns in the brush-tongued parrots (lories and lorikeets) of Australasia by sampling ultraconserved elements in 105 taxa. Trees estimated with low coverage sites had several clades where historical or modern samples clustered together, which were not observed in trees with more stringent filtering. To assess if the aberrant relationships were affected by missing data, we performed a targeted outlier analysis of sites and loci and a more general data reduction approach where we excluded sites based on a percentage of data completeness. The outlier analyses showed that 6.6% of total sites were driving the topological differences among trees built with and without low coverage sites, and at these sites, historical samples had 7.5x more missing data than modern ones. An examination of subclades identified loci biased by missing data, and the exclusion of these loci shifted phylogenetic relationships. Predictive modeling found that outlier analysis scores were not correlated with summary statistics of locus alignments, indicating that outlier loci do not have characteristics differing from other loci. Excluding missing data by percentage completeness indicated that sites with 70% completeness were necessary to avoid spurious relationships, but more stringent conditions of data completeness produced less-resolved trees. After accounting for biased loci and understanding the stability of relationships, we inferred a more robust phylogenetic hypothesis for lories and lorikeets.

evolutionary biology↗

Genomic divergence in allopatric Northern Cardinals of the North American warm deserts is associated with behavioral differentiation

Biogeographic barriers are thought to be important in initiating speciation through geographic isolation, but they rarely indiscriminately and completely reduce gene flow across the entire community. Understanding which species attributes regulate a barrier could help elucidate how speciation is initiated. Here, we investigated the association of behavioral isolation on population differentiation in Northern Cardinals (Cardinalis cardinalis) distributed across the Cochise Filter Barrier, a region of transitional habitat which separates the Sonoran and Chihuahuan deserts. Using genome-wide markers, we modeled demographic history by fitting the data to isolation and isolation-with-migration models. The best-fit model indicated that desert populations diverged in the mid-Pleistocene and there has been historically low, unidirectional gene flow into the Sonoran Desert. We then tested song recognition using reciprocal call-broadcast experiments to compare song recognition between deserts, controlling for song dialect changes within deserts. We found that male Northern Cardinals in both deserts were most aggressive to local songs and failed to recognize across-barrier songs. A correlation of genomic differentiation despite historic introgression and strong song discrimination is consistent with a model where speciation is initiated across a barrier and maintained by behavioral isolation.

evolutionary biology↗

Species delimitation and biogeography of the gnatcatchers and gnatwrens (Aves: Polioptilidae)

The New World avian family Polioptilidae (gnatcatchers and gnatwrens) is distributed from Argentina to Canada and includes 15 species and more than 60 subspecies. No study to date has evaluated phylogenetic relationships within this family and the historical pattern of diversification within the group remains unknown. Moreover, species limits, particularly in widespread taxa that show geographic variation, remain unclear. In this study, we delimited species and estimated phylogenetic relationships using multilocus data for the entire family. We then used the inferred diversity along with alternative taxonomic classification schemes to evaluate how lumping and splitting of both taxa and geographical areas influenced biogeographic inference. Species-tree analyses grouped Polioptilidae into four main clades: Microbates, Ramphocaenus, a Polioptila guianensis complex, and the remaining members of Polioptila. Ramphocaenus melanurus was sister to the clade containing M. cinereiventris and M. collaris, which formed a clade sister to all species within Polioptila. Polioptila was composed of two clades, the first of which included the P. guianensis complex; the other contained all remaining species in the genus. Using multispecies coalescent modeling, we inferred a more than 3-fold increase in species diversity, of which 87% represent currently recognized species or subspecies. Much of this diversity corresponded to subspecies that occur in the Neotropics. We identified three polyphyletic species, and delimited 4-6 previously undescribed candidate taxa. Probabilistic modeling of geographic ranges on the species tree indicated that the family likely had an ancestral origin in South America, with all three genera independently colonizing North America. Support for this hypothesis, however, was sensitive to the taxonomic classification scheme used and the number of geographical areas allowed. Our study proposes the first phylogenetic hypothesis for Polioptilidae and provides genealogical support for the reclassification of species limits. Species limits and the resolution of geographical areas that taxa inhabit influence the inferred spatial diversification history.

evolutionary biology↗

A positive association between population genetic differentiation and speciation rates in New World birds

Although an implicit assumption of speciation biology is that population differentiation is an important stage of evolutionary diversification, its true significance remains largely untested. If population differentiation within a species is related to its speciation rate over evolutionary time, the causes of differentiation could also be driving dynamics of organismal diversity across time and space. Alternatively, geographic variants might be short-lived entities with rates of formation that are unlinked to speciation rates, in which case the causes of differentiation would have only ephemeral impacts. Combining population genetics datasets including 17,746 individuals from 176 New World bird species with speciation rates estimated from phylogenetic data, we show that the population differentiation rates within species predict their speciation rates over long timescales. Although relatively little variance in speciation rate is explained by population differentiation rate, the relationship between the two is robust to diverse strategies of sampling and analyzing both population-level and species-level datasets. Population differentiation occurs at least three to five times faster than speciation, suggesting that most populations are ephemeral. Population differentiation and speciation rates are more tightly linked in tropical species than temperate species, consistent with a history of more stable diversification dynamics through time in the Tropics. Overall, our results suggest investigations into the processes responsible for population differentiation can reveal factors that contribute to broad-scale patterns of diversity.

evolutionary biology↗